Loss of Calpain 3 dysregulates store-operated calcium entry and its exercise response in mice.
Limb Girdle Muscular Dystrophy R1/2A
ORAI1
STIM1
calcium homeostasis
skeletal muscle
Journal
FASEB journal : official publication of the Federation of American Societies for Experimental Biology
ISSN: 1530-6860
Titre abrégé: FASEB J
Pays: United States
ID NLM: 8804484
Informations de publication
Date de publication:
31 Jul 2024
31 Jul 2024
Historique:
revised:
18
06
2024
received:
30
03
2024
accepted:
08
07
2024
medline:
20
7
2024
pubmed:
20
7
2024
entrez:
20
7
2024
Statut:
ppublish
Résumé
Limb-Girdle Muscular Dystrophy R1/2A (LGMD R1/2A) is caused by mutations in the CAPN3 gene encoding Calpain 3, a skeletal-muscle specific, Ca
Identifiants
pubmed: 39031532
doi: 10.1096/fj.202400697R
doi:
Substances chimiques
Calpain
EC 3.4.22.-
Capn3 protein, mouse
EC 3.4.22.-
Calcium
SY7Q814VUP
Muscle Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e23825Subventions
Organisme : Coalition to Cure Calpain 3 Foundation
ID : AGR00024098
Organisme : NIAMS NIH HHS
ID : P50 AR052646
Pays : United States
Informations de copyright
© 2024 The Author(s). The FASEB Journal published by Wiley Periodicals LLC on behalf of Federation of American Societies for Experimental Biology.
Références
Angelini C. Calpainopathy. In: Adam MP, Mirzaa GM, Pagon RA, et al., eds. GeneReviews®. University of Washington, Seattle; 1993.
Sorimachi H, Imajoh‐Ohmi S, Emori Y, et al. Molecular cloning of a novel mammalian calcium‐dependent protease distinct from both m‐ and μ‐types: specific expression of the mRNA in skeletal muscle. J Biol Chem. 1989;264:20106‐20111.
Ono Y, Shimada H, Sorimachi H, et al. Functional defects of a muscle‐specific calpain, p94, caused by mutations associated with limb‐girdle muscular dystrophy type 2A. J Biol Chem. 1998;273:17073‐17078.
Angelini C, Nardetto L, Borsato C, et al. The clinical course of calpainopathy (LGMD2A) and dysferlinopathy (LGMD2B). Neurol Res. 2010;32:41‐46.
Park HJ, Jang H, Lee JH, et al. Clinical and pathological heterogeneity of Korean patients with CAPN3 mutations. Yonsei Med J. 2016;57:173‐179.
Richard I, Hogrel JY, Stockholm D, et al. Natural history of LGMD2A for delineating outcome measures in clinical trials. Ann Clin Transl Neurol. 2016;3:248‐265.
Winckler PB, da Silva AMS, Coimbra‐Neto AR, et al. Clinicogenetic lessons from 370 patients with autosomal recessive limb‐girdle muscular dystrophy. Clin Genet. 2019;96:341‐353.
de Paula F, Vainzof M, Passos‐Bueno MR, et al. Clinical variability in calpainopathy: what makes the difference? Eur J Hum Genet. 2002;10:825‐832.
Martinez‐Thompson JM, Moore SA, Liewluck T. A novel CAPN3 mutation in late‐onset limb‐girdle muscular dystrophy with early respiratory insufficiency. J Clin Neurosci. 2018;53:229‐231.
Ono Y, Torii F, Ojima K, et al. Suppressed disassembly of autolyzing p94/CAPN3 by N2A connectin/titin in a genetic reporter system. J Biol Chem. 2006;281:18519‐18531.
Ono Y, Sorimachi H, Suzuki K. New aspect of the research on limb‐girdle muscular dystrophy 2A: a molecular biologic and biochemical approach to pathology. Trends Cardiovasc Med. 1999;9:114‐118.
Richard I, Broux O, Allamand V, et al. Mutations in the proteolytic enzyme Calpain 3 cause limb‐girdle muscular dystrophy type 2A. Cell. 1995;81:27‐40.
Kramerova I, Beckmann JS, Spencer MJ. Molecular and cellular basis of calpainopathy (limb girdle muscular dystrophy type 2A). Biochim Biophys Acta. 2007;1772:128‐144.
Kramerova I, Kudryashova E, Wu B, Ottenheijm C, Granzier H, Spencer MJ. Novel role of calpain‐3 in the triad‐associated protein complex regulating calcium release in skeletal muscle. Hum Mol Genet. 2008;17:3271‐3280.
Dulhunty AF, Wei‐LaPierre L, Casarotto MG, Beard NA. Core skeletal muscle ryanodine receptor calcium release complex. Clin Exp Pharmacol Physiol. 2017;44:3‐12.
Ojima K, Ono Y, Ottenheijm C, et al. Non‐proteolytic functions of Calpain‐3 in sarcoplasmic reticulum in skeletal muscles. J Mol Biol. 2011;407:439‐449.
Fanin M, Angelini C. Protein and genetic diagnosis of limb girdle muscular dystrophy type 2A: the yield and the pitfalls. Muscle Nerve. 2015;52:163‐173.
DiFranco M, Kramerova I, Vergara JL, Spencer MJ. Attenuated Ca2+ release in a mouse model of limb girdle muscular dystrophy 2A. Skelet Muscle. 2016;6:11.
Toral‐Ojeda I, Aldanondo G, Lasa‐Elgarresta J, et al. Calpain 3 deficiency affects SERCA expression and function in the skeletal muscle. Expert Rev Mol Med. 2016;18:e7.
Kramerova I, Kudryashova E, Ermolova N, et al. Impaired calcium calmodulin kinase signaling and muscle adaptation response in the absence of Calpain 3. Hum Mol Genet. 2012;21:3193‐3204.
Boncompagni S, Michelucci A, Pietrangelo L, Dirksen RT, Protasi F. Exercise‐dependent formation of new junctions that promote STIM1‐Orai1 assembly in skeletal muscle. Sci Rep. 2017;7:14286.
Wei‐LaPierre L, Carrell EM, Boncompagni S, Protasi F, Dirksen RT. Orai1‐dependent calcium entry promotes skeletal muscle growth and limits fatigue. Nat Commun. 2013;4:2805.
Edwards JN, Murphy RM, Cully TR, von Wegner F, Friedrich O, Launikonis BS. Ultra‐rapid activation and deactivation of store‐operated Ca(2+) entry in skeletal muscle. Cell Calcium. 2010;47:458‐467.
Michelucci A, Boncompagni S, Pietrangelo L, et al. Transverse tubule remodeling enhances Orai1‐dependent Ca2+ entry in skeletal muscle. elife. 2019;8:e47576.
Michelucci A, Boncompagni S, Pietrangelo L, Takano T, Protasi F, Dirksen RT. Pre‐assembled Ca2+ entry units and constitutively active Ca2+ entry in skeletal muscle of calsequestrin‐1 knockout mice. J Gen Physiol. 2020;152:e202012617.
Edwards JN, Friedrich O, Cully TR, von Wegner F, Murphy RM, Launikonis BS. Upregulation of store‐operated Ca2+ entry in dystrophic mdx mouse muscle. Am J Physiol Cell Physiol. 2010;299:C42‐C50.
Goonasekera SA, Davis J, Kwong JQ, et al. Enhanced Ca2+ influx from STIM1–Orai1 induces muscle pathology in mouse models of muscular dystrophy. Hum Mol Genet. 2014;23:3706‐3715.
Garcia‐Castaneda M, Michelucci A, Zhao N, Malik S, Dirksen RT. Postdevelopmental knockout of Orai1 improves muscle pathology in a mouse model of Duchenne muscular dystrophy. J Gen Physiol. 2022;154:e202213081.
Kramerova I, Kudryashova E, Tidball JG, Spencer MJ. Null mutation of Calpain 3 (p94) in mice causes abnormal sarcomere formation in vivo and in vitro. Hum Mol Genet. 2004;13:1373‐1388.
Mizunoya W, Wakamatsu J‐I, Tatsumi R, Ikeuchi Y. Protocol for high‐resolution separation of rodent myosin heavy chain isoforms in a mini‐gel electrophoresis system. Anal Biochem. 2008;377:111‐113.
Kim J‐K, Jha NN, Feng Z, et al. Muscle‐specific SMN reduction reveals motor neuron–independent disease in spinal muscular atrophy models. J Clin Invest. 2020;130:1271‐1287.
Moorwood C, Barton ER. Caspase‐12 ablation preserves muscle function in the mdx mouse. Hum Mol Genet. 2014;23:5325‐5341.
Michelucci A, Pietrangelo L, Rastelli G, Protasi F, Dirksen RT, Boncompagni S. Constitutive assembly of Ca2+ entry units in soleus muscle from calsequestrin knockout mice. J Gen Physiol. 2022;154:e202213114.
Launikonis BS, Ríos E. Store‐operated Ca2+ entry during intracellular Ca2+ release in mammalian skeletal muscle. J Physiol. 2007;583:81‐97.
Lyfenko AD, Dirksen RT. Differential dependence of store‐operated and excitation‐coupled Ca2+ entry in skeletal muscle on STIM1 and Orai1. J Physiol. 2008;586:4815‐4824.
Wang CH, Liang WC, Minami N, Nishino I, Jong YJ. Limb‐girdle muscular dystrophy type 2a with mutation in CAPN3: the first report in Taiwan. Pediatr Neonatol. 2015;56:62‐65.
Kramerova I, Ermolova N, Eskin A, et al. Failure to up‐regulate transcription of genes necessary for muscle adaptation underlies limb girdle muscular dystrophy 2A (calpainopathy). Hum Mol Genet. 2016;25:2194‐2207.
Ono Y, Ojima K, Shinkai‐Ouchi F, Hata S, Sorimachi H. An eccentric calpain, CAPN3/p94/calpain‐3. Biochimie. 2016;122:169‐187.
Richard I, Roudaut C, Saenz A, et al. Calpainopathy‐a survey of mutations and polymorphisms. Am J Hum Genet. 1999;64:1524‐1540.
Barton ER, Pacak CA, Stoppel WL, Kang PB. The ties that bind: functional clusters in limb‐girdle muscular dystrophy. Skelet Muscle. 2020;10:22.
Baghdiguian S, Martin M, Richard I, et al. Calpain 3 deficiency is associated with myonuclear apoptosis and profound perturbation of the IκBα/NF‐κB pathway in limb‐girdle muscular dystrophy type 2A. Nat Med. 1999;5:503‐511.
Boncompagni S, Pozzer D, Viscomi C, Ferreiro A, Zito E. Physical and functional cross talk between endo‐sarcoplasmic reticulum and mitochondria in skeletal muscle. Antioxid Redox Signal. 2020;32:873‐883.
Kramerova I, Kudryashova E, Wu B, et al. Mitochondrial abnormalities, energy deficit and oxidative stress are features of Calpain 3 deficiency in skeletal muscle. Hum Mol Genet. 2009;18:3194‐3205.
Sztretye M, Singlár Z, Balogh N, et al. The role of Orai1 in regulating sarcoplasmic calcium release, mitochondrial morphology and function in myostatin deficient skeletal muscle. Front Physiol. 2020;11:601090.
Protasi F, Pietrangelo L, Boncompagni S. Calcium entry units (CEUs): perspectives in skeletal muscle function and disease. J Muscle Res Cell Motil. 2021;42:233‐249.
Vallejo‐Illarramendi A, Toral‐Ojeda I, Aldanondo G, López de Munain A. Dysregulation of calcium homeostasis in muscular dystrophies. Expert Rev Mol Med. 2014;16:e16.
Pollitt C, Anderson LV, Pogue R, Davison K, Pyle A, Bushby KM. The phenotype of calpainopathy: diagnosis based on a multidisciplinary approach. Neuromuscul Disord. 2001;11:287‐296.
Carrell EM, Coppola AR, McBride HJ, Dirksen RT. Orai1 enhances muscle endurance by promoting fatigue‐resistant type I fiber content but not through acute store‐operated Ca2+ entry. FASEB J. 2016;30:4109‐4119.
Saint‐Martin Willer A, Montani D, Capuano V, Antigny F. Orai1/STIMs modulators in pulmonary vascular diseases. Cell Calcium. 2024;121:102892.
Dayanithi G, Richard I, Viero C, et al. Alteration of sarcoplasmic reticulum Ca2+ release in skeletal muscle from Calpain 3‐deficient mice. Int J Cell Biol. 2009;2009:340346.
Milic A, Daniele N, Lochmüller H, et al. A third of LGMD2A biopsies have normal Calpain 3 proteolytic activity as determined by an in vitro assay. Neuromuscul Disord. 2007;17:148‐156.
Ermolova N, Kudryashova E, DiFranco M, Vergara J, Kramerova I, Spencer MJ. Pathogenity of some limb girdle muscular dystrophy mutations can result from reduced anchorage to myofibrils and altered stability of Calpain 3. Hum Mol Genet. 2011;20:3331‐3345.